International Journal of Biometeorology

, Volume 58, Issue 4, pp 419–426 | Cite as

Within-season flowering interruptions are common in the water-limited Sky Islands

  • Theresa M. CrimminsEmail author
  • C. David Bertelsen
  • Michael A. Crimmins
Phenology – Milwaukee 2012


Within-season breaks in flowering have been reported in a wide range of highly variable ecosystems including deserts, tropical forests and high-elevation meadows. A tendency for interruptions in flowering has also been documented in southwestern US “Sky Island” plant communities, which encompass xeric to mesic conditions. Seasonal breaks in flowering have implications for plant reproductive success, population structure, and gene flow as well as resource availability for pollinators and dependent animals. Most reports of multiple within-season flowering events describe only two distinct flowering episodes. In this study, we set out to better quantify distinct within-season flowering events in highly variable Sky Islands plant communities. Across a >1,200 m elevation gradient, we documented a strong tendency for multiple within-season flowering events. In both distinct spring and summer seasons, we observed greater than two distinct within-season flowering in more than 10 % of instances. Patterns were clearly mediated by the different climate factors at work in the two seasons. The spring season, which is influenced by both temperature and precipitation, showed a mixed response, with the greatest tendency for multiple flowering events occurring at mid-elevations and functional types varying in their responses across the gradient. In the summer season, during which flowering across the gradient is limited by localized precipitation, annual plants exhibited the fewest within-season flowering events and herbaceous perennial plants showed the greatest. Additionally, more distinct events occurred at lower elevations. The patterns documented here provide a baseline for comparison of system responses to changing climate conditions.


Arid Elevation gradient Flowering phenology Interrupted flowering Phenology Semi-arid Water-limited 



We are thankful to the staff and associated researchers of the University of Arizona Herbarium for assistance with plant identification. We are also grateful to J.F. Weltzin, A.H. Rosemartin, and the staff of the USA National Phenology Network National Coordinating Office, who are consistently supportive of this research and frequently provide thoughtful comments and suggestions. We also sincerely appreciate M. Borgstrom’s guidance with statistical tests. Finally, this manuscript was dramatically improved by the input from two anonymous reviewers.


  1. Aronson J, Kigel J, Shmida A, Klein J (1992) Adaptive phenology of desert and Mediterranean populations of annual plants grown with and without water stress. Oecologia 89:17–26CrossRefGoogle Scholar
  2. Augspurger CK (1983) Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15:257–267CrossRefGoogle Scholar
  3. Bawa KS, Kang H, Grayum MH (2003) Relationships among time, frequency, and duration of flowering in tropical rain forest trees. Am J Bot 90:877–887CrossRefGoogle Scholar
  4. Bowers JE, Dimmit MA (1994) Flowering phenology of six woody plants in the northern Sonoran Desert. B Torrey Bot Club 121:215–229CrossRefGoogle Scholar
  5. Bronstein JL (1995) The plant-pollinator landscape. In: Hansson L, Fahrig L, Merriam G (eds) Mosaic landscapes and ecological processes. Chapman & Hall London, pp 256–288Google Scholar
  6. Brown DE (1982) Biotic communities: southwestern United States and northwestern Mexico. University of Utah Press, Salt Lake CityGoogle Scholar
  7. Bullock SH, Solis-Magallanes JA (1990) Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica 22:22–35CrossRefGoogle Scholar
  8. Burgess TL (1995) Desert grassland, mixed shrub savanna, shrub steppe, or semidesert scrub? In: McClaran MP, Van Devender TR (eds) The desert grassland. The University of Arizona Press, Tucson, pp 31–67Google Scholar
  9. Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function. Science 339:1611–1615. doi: 10.1126/science.1232728 Google Scholar
  10. Crimmins TM, Crimmins MA, Bertelsen CD, Balmat J (2008) Relationships between alpha diversity of plant species in bloom and climatic variables across an elevation gradient. Int J Biometeorol 52:353–366CrossRefGoogle Scholar
  11. Crimmins TM, Crimmins MA, Bertelsen CD (2010) Complex responses to climate drivers in onset of spring flowering across a semi-arid elevation gradient. J Ecol 98:1042–1051CrossRefGoogle Scholar
  12. Crimmins TM, Crimmins MA, Bertelsen CD (2011) Onset of summer flowering in a ‘Sky Island’ is driven by monsoon moisture. New Phytol 191:468–479CrossRefGoogle Scholar
  13. Crimmins TM, Crimmins MA, Bertelsen CD (2013) Spring and summer patterns in flowering onset, duration, and constancy across a water-limited gradient. Am J Bot 100(6):1–11CrossRefGoogle Scholar
  14. Ehleringer J (1985) Comparative microclimatology and plant responses in Encelia species from contrasting habitats. J Arid Environ 8:45–56Google Scholar
  15. Ehleringer JR, Phillips SL, Schuster WSF, Sandquist DR (1991) Differential utilization of summer rains by desert plants. Oecologia 88:430–434CrossRefGoogle Scholar
  16. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439CrossRefGoogle Scholar
  17. Etheredge D, Gutzler DS, Pazzaglia FJ (2004) Geomorphic response to seasonal variations in rainfall in the Southwest United State. Geol Soc Am Bull 116:606–618CrossRefGoogle Scholar
  18. Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919CrossRefGoogle Scholar
  19. Goodrich DC, Faures J, Woolhiser DA, Lane L, Sorooshian S (1995) Measurement and analysis of small-scale convective storm rainfall variability. J Hydrol 173:283–308CrossRefGoogle Scholar
  20. Hunter RB (1989) Competition between adult and seedling shrubs of Ambrosia dumosa in the Mojave Desert Great Basin. Nature 49:79–84Google Scholar
  21. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362CrossRefGoogle Scholar
  22. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112CrossRefGoogle Scholar
  23. Llorens L, Peñuelas J (2005) Experimental evidence of future drier and warmer conditions affecting flowering of two co-occurring Mediterranean shrubs. Int J Plant Sci 166:235–245CrossRefGoogle Scholar
  24. MacMahon JA, Schimpf DJ (1981) Water as a factor in the biology of North American desert plants. In: Evans DD, Thames JL (eds) Water in desert ecosystems. Dowden, Hutchinson, Ross, Stroudsburg, PA, pp 114–171Google Scholar
  25. MacMahon JA, Wagner FH (1985) The Mojave, Sonoran and Chihuahuan Deserts of North America. In: Evenari M, Noy-Meir I, Goodall DW (eds) Hot deserts and arid shrublands. Ecosystems of the world, vol 12A. Elsevier, Amsterdam, pp 105–202Google Scholar
  26. Maestre FT, Salguero-Gómez R, Quero JL (2012) It is getting hotter in here: determining and projecting the impacts of global environmental change on drylands. Philos Trans R Soc B 367:3062–3075CrossRefGoogle Scholar
  27. McGinnies WG (1981) Discovering the desert. University of Arizona Press, TucsonGoogle Scholar
  28. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717CrossRefGoogle Scholar
  29. Miller-Rushing AJ, Inouye DW (2009) Variation in the impact of climate change on flowering phenology and abundance: an examination of two pairs of closely related wildflower species. Am J Bot 96:1821–1829CrossRefGoogle Scholar
  30. Newstrom LE, Frankie GW, Baker HG, Colwell RK (1994) Diversity of long-term flowering patterns. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: Ecology and natural history of a neotropical rain forest. University of Chicago Press, Chicago, pp 142–160Google Scholar
  31. Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:23–51CrossRefGoogle Scholar
  32. Oleson JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582CrossRefGoogle Scholar
  33. Opler PA, Frankie GW, Baker HG (1976) Rainfall as a factor in the release, timing, and asynchronization of anthesis by tropical trees and shrubs. J Biogeogr 3:231–236CrossRefGoogle Scholar
  34. Prieto P, Peñuelas J, Ogaya R, Estiarte M (2008) Precipitation-dependent flowering of Globularia alypum and Erica multiflora in Mediterranean shrubland under experimental drought and warming, and its inter-annual variability. Ann Bot 102:275–285CrossRefGoogle Scholar
  35. Reynolds JF, Kemp PR, Tenhunen JD (2000) Effects of long-term rainfall variability on evapotranspiration and soil water distribution in the Chihuahuan Desert: a modeling analysis. Plant Ecol 150:145–159CrossRefGoogle Scholar
  36. Reynolds JF, Kemp PR, Ogle K (2004) Modifying the ‘pulse-reserve’ paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141:194–210CrossRefGoogle Scholar
  37. Sala OE, Lauenroth WK (1985) Root profiles and the ecological effect of light rainshowers in arid and semiarid regions. Am Midl Nat 114:406–408CrossRefGoogle Scholar
  38. Salguero-Gómez R, Siewert W, Casper BB, Tielbörger K (2012) A demographic approach to study effects of climate change in desert plants. Philos Trans R Soc B 367:3100–3114CrossRefGoogle Scholar
  39. Scaven VL, Rafferty NE (2013) Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59:418–426Google Scholar
  40. Shreve F (1951) Vegetation of the Sonoran Desert. Carnegie Institution of Washington, Washington, DCGoogle Scholar
  41. Smith SD, Nowak RS (1990) Ecophysiology of plants in the intermountain lowlands. In: Osmond CB, Pitelka LF, Hidy M (eds) Plant biology of the basin and range. Springer, Berlin, pp 179–241CrossRefGoogle Scholar
  42. Smith SD, Monson RK, Anderson JE (1997) Physiological ecology of North American desert plants. Springer, BerlinCrossRefGoogle Scholar
  43. Solbrig OT, Orians GH (1977) The adaptive characteristics of desert plants: a cost/benefit analysis of photosynthesis leads to predictions about the types and distributions of desert plants. Am Sci 65:412–421Google Scholar
  44. Szarek SR, Woodhouse RM (1976) Ecophysiological studies of Sonoran Desert plants. I. Diurnal photosynthesis patterns of Ambrosia deltoidea and Olneya tesota. Oecologia 26:225–234CrossRefGoogle Scholar
  45. Tevis L (1958) Germination and growth of ephemerals induced by sprinkling in a sandy desert. Ecology 39:681–688CrossRefGoogle Scholar
  46. Venable DL, Pake CE (1999) Population ecology of Sonoran Desert annual plants. In: Robichaux RB (ed) The ecology of Sonoran Desert plants and plant communities. University of Arizona Press, Tucson, pp 115–142Google Scholar
  47. Walter H (1971) Natural savannahs as a transition to the arid zone. In: Ecology of tropical and subtropical vegetation. Oliver & Boyd, Edinburgh, pp 238–265Google Scholar
  48. Went FW (1948) Ecology of desert plants. I. Observations on germination in the Joshua Tree National Monument, California. Ecology 29:242–253CrossRefGoogle Scholar
  49. Went FW (1949) Ecology of desert plants. II. The effect of rain and temperature on germination and growth. Ecology 30:1–13CrossRefGoogle Scholar
  50. Went FW (1957) The experimental control of plant growth. Varronica Botanica, WalthamGoogle Scholar
  51. Whittaker RH, Niering WA (1965) Vegetation of the Santa Catalina Mountains, Arizona: a gradient analysis of the south slope. Ecology 46:429–452CrossRefGoogle Scholar
  52. Whittaker RH, Buol SW, Niering WA, Havens YH (1968) A soil and vegetation pattern in the Santa Catalina Mountains, Arizona. Soil Sci 105:440–450CrossRefGoogle Scholar
  53. Xavier-Picó F, Retana J (2001) The flowering pattern of the perennial herb Lobularia maritima: an unusual case in the Mediterranean basin. Acta Oecol 22:209–217CrossRefGoogle Scholar

Copyright information

© ISB 2013

Authors and Affiliations

  • Theresa M. Crimmins
    • 1
    • 2
    Email author
  • C. David Bertelsen
    • 2
    • 3
  • Michael A. Crimmins
    • 4
  1. 1.USA National Phenology NetworkTucsonUSA
  2. 2.School of Natural Resources and the EnvironmentUniversity of ArizonaTucsonUSA
  3. 3.HerbariumUniversity of ArizonaTucsonUSA
  4. 4.Department of Soil, Water and Environmental ScienceUniversity of ArizonaTucsonUSA

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